Controversies of the origin of life

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INTERNATIONAL MICROBIOLOGY (2005) 8:23-31 www.im.microbios.org

Juli Peretó
Cavanilles Institute for Biodiversity and Evolutionary Biology, and Department of Biochemistry and Molecular Biology, University of Valencia, Spain

Controversies on the origin of life
Summary. Different viewpoints, many with deep philosophical and historical roots, have shaped the scientific studyof the origin of life. Some of these argue that primeval life was based on simple anaerobic microorganisms able to use a wide inventory of abiotic organic materials (i.e. a heterotrophic origin), whereas others invoke a more sophisticated organization, one that thrived on simple inorganic molecules (i.e. an autotrophic origin). While many scientists assume that life started as a self-replicativemolecule, the first gene, a primitive self-catalytic metabolic network has also been proposed as a starting point. Even the emergence of the cell itself is a contentious issue: did boundaries and compartments appear early or late during life's origin? Starting with a recent definition of life, based on concepts of autonomy and open-ended evolution, it is proposed here that, firstly, organicmolecules self-organized in a primordial metabolism located inside protocells. The flow of matter and energy across those early molecular systems allowed the generation of more ordered states, forming the cradle of the first genetic records. Thus, the origin of life was a process initiated within ecologically interconnected autonomous compartments that evolved into cells with hereditary and true Darwinianevolutionary capabilities. In other words, the individual existence of life preceded its historical-collective dimension. [Int Microbiol 2005; 8(1):23-31] Key words: autonomy · life definition · open-ended evolution · protocells

Received 4 February 2005 Accepted 18 February 2005 Address for correspondence: Institut Cavanilles de Biodiversitat i Biologia Evolutiva Poligon de la Coma, s/nE-46980 Paterna, Spain Tel. +34-963543666. Fax +34-963543670 E-mail: juli.pereto@uv.es

Introduction
Life is matter with two biographies: (i) ontogenetic, synchronic, developmental, individual existence, based on the autopoietic (i.e. self-building) properties of cells and their ecological (i.e. biogeochemical) consequences, and (ii) the historical-collective, diachronic, populational, evolutionaryprocess. Metabolism and genetics are the two central pillars that sustain life. Every living being uses external sources of both energy and matter to fight against disorder, equilibrium, and death. Membranes and molecular machines located on the frontier between the inside and the outside control and manage flows of energy and matter for the benefit of the cell

itself. In current life forms,those activities are dependent on digital genetic records. Change, acquisition, and loss of fragments of the informative molecules are the basic mechanisms of evolution, i.e. the differential capacity for adaptation, survival, and reproduction. The historical persistence of genetic records depends absolutely on the metabolic and ecological abilities of organisms. A fundamental question is thus howthe metabolic and genetic functions, which in terrestrial life forms are so intricately intertwined, came to be an integral part of the history of this planet. Which came first, the autopoietic or the hereditary properties of living matter?

What is life?
Although defining life is a difficult task, we recently proposed a definition that tries to join in a compact sentence both biographicalaspects: “a living being is any autonomous

This article is dedicated to the memory of three illuminating scientists recently deceased: Ramon Margalef (1919-2004), Joan Oró (1923-2004) and Alfred Giner-Sorolla (1919-2005).

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system with open-ended evolutionary capacities” [34]. The term “autonomy” refers to the relationship between the living being...
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